The game's story takes place during the year 1797, 5 years after the events of Rondo of Blood and begins with Richter Belmont's defeat of Count Dracula, mirroring the end of the former game. However, despite Dracula being defeated, Richter vanishes without a trace. Castlevania rises again five years later, and while there are no Belmonts to storm the castle, Alucard, the son of Dracula, awakens from his self-induced sleep, and decides to investigate what transpired during his slumber.

Meanwhile, Maria Renard, Richter's sister-in-law, enters Castlevania herself to search for the missing Richter. She assists Alucard multiple times throughout the game.